International Journal of

Molecular Sciences

Review

Bacterial Cellulose—Graphene Based Nanocomposites

Omar P. Troncoso and Fernando G. Torres *

Department of Mechanical Engineering, Pontificia Universidad Católica del Perú, Lima 15088, Peru;troncoso.op@pucp.pe* Correspondence: fgtorres@pucp.pe; Tel.: +511-626-2000

Received: 1 August 2020; Accepted: 2 September 2020; Published: 7 September 2020�����������������

Abstract: Bacterial cellulose (BC) and graphene are materials that have attracted the attention ofresearchers due to their outstanding properties. BC is a nanostructured 3D network of pure and highlycrystalline cellulose nanofibres that can act as a host matrix for the incorporation of other nano-sizedmaterials. Graphene features high mechanical properties, thermal and electric conductivity andspecific surface area. In this paper we review the most recent studies regarding the developmentof novel BC-graphene nanocomposites that take advantage of the exceptional properties of BC andgraphene. The most important applications of these novel BC-graphene nanocomposites includethe development of novel electric conductive materials and energy storage devices, the preparationof aerogels and membranes with very high specific area as sorbent materials for the removal of oiland metal ions from water and a variety of biomedical applications, such as tissue engineering anddrug delivery. The main properties of these BC-graphene nanocomposites associated with theseapplications, such as electric conductivity, biocompatibility and specific surface area, are systematicallypresented together with the processing routes used to fabricate such nanocomposites.

Keywords: bacterial cellulose; graphene; supercapacitors; biomedical applications; water purification

1. Introduction

Cellulose is an abundant inexpensive biopolymer, traditionally extracted from plants and biomasswaste. The cellulose synthetized by plants is usually branched with hemicellulose and lignin. It has toundergo chemical process to obtain the pure cellulose [1]. Some acetic acid bacteria can synthetizecellulose extracellularly. This bacterial cellulose (BC) is formed only by glucose monomers withouthemicellulose or lignin. Glucose chain protofibrils are secreted through bacteria cell wall and aggregatetogether forming nanofibrils cellulose ribbons [2]. These cellulose ribbons aggregate themselves toform a coherent 3D cellulose network. As a result, a pellicle with high surface area and porosity isformed. This cellulose nanofibre network has high mechanical strength, high crystallinity, high degreeof polymerization and high water holding capacity. Table 1 summarizes some of the most importantproperties of BC network.

Pure BC features uncontrolled hydrolysis rate and low biological activity. BC-based nanocompositeshave been developed to improve the capabilities of pure BC. BC nanocomposites have been used for thedevelopment of high strength paper and polymeric films, high strength membranes and as a reinforcingagent for polymer nanocomposites [3]. In addition, due to its non-toxicity and biocompatibility,BC-based materials have also been used for biomedical applications such as biological implants,artificial blood vessels for microsurgery, scaffolds for tissue engineering and wound dressing patches,among others [4].

Graphene is another nanomaterial that has attracted extensive interest due to its outstandingphysicochemical properties, including high Young’s modulus, high electrical and thermal conductivity,quick charge carrier mobility and large specific surface area (Table 1). Graphene is the first truly two

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dimensional (2D) crystal ever discovered [5,6]. A graphene crystal is composed of six-atom ringsin a honeycombed network with one-atom thickness, forming a free-standing 2-D crystal that canfunction as a planar aromatic macromolecule [7]. Each carbon atom is bonded to three other carbonatoms, forming three σ-bonds via three sp2 hybrid orbitals. The other p-orbital form a conjugatedsystem with other contiguous carbon atoms. As a result, the carbon skeleton of graphene is made ofσ-bonds with paired electron clouds above and below the skeleton. Graphene can be transformed intospherical structures (0-D fullerenes), tubular structures (one-dimensional carbon nanotubes, 1-D CNTs)or layered structures (3-D graphite) [8]. Graphene, graphene oxide (GO) and reduced grapheneoxide (RGO) have found a variety of applications in quantum physics, nanoelectronics, catalysis,nanocomposites and sensor technology [9–13].

Pristine graphene was first obtained in 2004, by exfoliating highly oriented pyrolytic graphite [5].Other processing techniques have been developed in order to increase the productivity and reduce thecost of graphene. These techniques have allowed for the fabrication of a variety of graphene familynanomaterials (GFNs). Among them, graphene oxide (GO) and reduced graphene oxide (RGO) are themost commonly used.

GO is usually obtained by chemical exfoliation following the Hummers method [14]. Briefly,graphite and NaNO3 are added to concentrated sulfuric acid, followed by KMnO4 as the oxidizingagent to oxidize the graphite. Then, 30% H2O2 is added to reduce the oxidizing agent and obtain GO.However, GO has not the same properties as graphene. GO is hydrophilic and electrically insulating.During the chemical exfoliation of graphite, a significant fraction of the sp2 carbon network is bondedwith oxygen-containing hydrophilic groups. This causes the disruption of the sp2 bonding networkin its carbon basal plane [15–17]. Thus, for some applications the GO has to be reduced in order torestore some of the properties of pristine graphene. There are a variety of processing routes to reduceGO, including chemical reduction, photocatalytic reduction, electrochemical reduction and thermalreduction [18–21].

Table 1. Summary of bacterial cellulose (BC) and graphene properties.

Properties Value Observation References

Bacterial cellulose network

Diameter 35–90 nm Individual nanofibres [22]Length 580–960 µm Individual nanofibres [23]

Young’s modulus 78 GPa Individual nanofibres [22]Porosity 65–75% BC native network hydrogel [24]

Surface area 20 m2/g BC native network hydrogel [25]Water holding capacity 201% BC native network hydrogel [25]

Graphene

Surface area 2600 m2/g Theoretical prediction [26]Mobility 15,000 cm2 V−1 s−1 Room temperature [26]

Electric conductivity 106–107 S m−1 Isolated single particle conductivity [27]Thermal conductivity 5.8 × 103 Wm−1K−1 - [26]

Young’s modulus 1 TPa - [26]

BC is a biopolymer that forms nanostructured 3D network with outstanding mechanical properties.This BC network can be used as matrix for the development of novel nanocomposites with tailoredproperties. On the other hand, GFNs features remarkable properties such as thermal and electronicconductivity as well as high mechanical properties. This review offers an overview of the most recentBC-graphene nanocomposites developed to take advantage of the exceptional properties of BC andGFNs. Three main applications were identified for these BC-GFN nanocomposites, including thedevelopment of novel electric conductive materials and energy storage devices, the preparation ofaerogels and membranes with very high specific area as sorbent materials for the removal of oil andmetal ions from water and a variety of biomedical applications, such as tissue engineering and drug

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delivery. The main properties of these BC-GFN nanocomposites associated with these applications,such as electric conductivity, biocompatibility and specific surface area, are systematically presentedtogether with the processing routes used to fabricate such nanocomposites. This review can be used asa guide to support researchers for the development of novel graphene- and cellulose- based materialsfor different applications including green electronic devices, water purification systems and biomedicalmaterials, among other applications that have not been considered yet.

2. Processing Routes

Bacterial cellulose can be synthetized by different bacteria, including Gram negative bacteriasuch as Gluconacetobacter xylinus [23,28], Agrobacterium [29], Rhizobium [30] and Gram positive bacteriasuch as Sarcina [31]. The preparation of BC-based nanocomposites includes a culture step for bacterialgrowth. Different culture media have been used to improve the cellulose synthesis.

Mohammadkazemi et al. [32] compared the effects of using different carbon sources and growmedia. The carbon sources they used were syrup, glucose, mannitol and sucrose while the grow mediawere the Hestrin–Schramm, Yamanaka and Zhou media. They found that mannitol lead to the highestyield and that the crystallinity of the BC in presence of the Hestrin–Schramm medium had highervalues than those from other media. The culture of bacteria is normally carried out in static conditionsbut some studies have used agitated conditions. When BC is cultivated in static conditions, a cellulosepellicle is formed at the medium surface exposed to air, while in agitated condition; the spherical orasterisk-like shape cellulose particles are obtained [33].

These pellicles are formed by a cellulose network made from fibres having ~100 nm in diameter [4].When combining BC with another nano-sized element the developed material can be regarded asa nano-nano composite. Many different processing routes have been reported for the preparationof BC-based nano-nano composites, including BC-Graphene nanocomposites [3]. When preparingBC-Graphene nanocomposites, there are two important aspects that need to be considered. Firstly,we need to consider if the pristine BC network structure has to be preserved. When the BC networkremains undisturbed, the resulting nanocomposites take advantage of the intrinsic mechanicalrobustness of pristine BC. However, the incorporation of a second phase into this cellulose network canbe a challenging task and, thus, the disintegration of BC has also been used as a strategy to combineBC and graphene.

The second aspect to be considered is how the graphene platelets are incorporated into the BCnetwork. Graphene can be incorporated after the cellulose fibres have been synthetized or duringthe cellulose synthesis. For instance, one common way of incorporating graphene is by immersing apristine BC pellicle in graphene dispersion [34]. A different approach consists in modifying the culturemedium of bacteria adding a graphene dispersion in order to allow the synthesis of cellulose in thepresence of graphene platelets. As a result, a BC pellicle containing graphene platelets is obtained.

Figure 1 shows three of the most common processing routes used for the preparation of BC-GOnanocomposites. In the first and second routes, BC synthesis is carried out in an unmodified mediumand a BC pellicle is obtained. Then, this BC pellicle can be either disintegrated (Figure 1a) or preserved(Figure 1b). The BC is disintegrated by means of a homogenizer or pulping equipment and a BC slurryis obtained [35–40]. This BC slurry is then combined with a GO dispersion. Usually, a sonication orsome other process is used to achieve a homogenous dispersion. Then, the BC-GO dispersion is dried,pressed or filtered to form a solid film. When the network structure of BC is preserved (Figure 1b) GOis incorporated by an impregnation step and, then, the BC pellicle with the GO incorporated is dried orpressed. Alternatively, a GO dispersion is poured on a BC pellicle and vacuum-dried to incorporateBC and obtain a film in a single step.

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Figure 1 shows three of the most common processing routes used for the preparation of BC-GO nanocomposites. In the first and second routes, BC synthesis is carried out in an unmodified medium and a BC pellicle is obtained. Then, this BC pellicle can be either disintegrated (Figure 1a) or preserved (Figure 1b). The BC is disintegrated by means of a homogenizer or pulping equipment and a BC slurry is obtained [35–40]. This BC slurry is then combined with a GO dispersion. Usually, a sonication or some other process is used to achieve a homogenous dispersion. Then, the BC-GO dispersion is dried, pressed or filtered to form a solid film. When the network structure of BC is preserved (Figure 1b) GO is incorporated by an impregnation step and, then, the BC pellicle with the GO incorporated is dried or pressed. Alternatively, a GO dispersion is poured on a BC pellicle and vacuum-dried to incorporate BC and obtain a film in a single step.

Figure 1. Processing routes reported for the preparation of BC- graphene oxide (GO) nanocomposites. In the first route, the pure BC membrane is disintegrated and a GO-BC suspension is prepared in order to prepare a composite BC-GO film (a). In the second route, GO is incorporated into the preserved BC network (b). In the third processing route, the BC growing medium is modified by the addition of a GO suspension and the BC network is synthetized in the presence of GO (c). For the fourth processing route a conventional growing medium is used to grow a first BC pellicle. Then, a modified growing medium is prepared adding a GO suspension. This modified medium is sprayed onto the first BC pellicle forming a thin layer of culture medium on which new BC nanofibres are synthetized in presence of GO (d).

For instance, Fang et al. [35] prepared BC-GO membranes following the first route (Figure 1a) for selective ion permeation. They dried and disintegrated the pristine BC pellicle. Then, they dispersed it in formamide with sonication for 2 h at 400 W to prepare stable BC dispersion with

Figure 1. Processing routes reported for the preparation of BC- graphene oxide (GO) nanocomposites.In the first route, the pure BC membrane is disintegrated and a GO-BC suspension is prepared in orderto prepare a composite BC-GO film (a). In the second route, GO is incorporated into the preserved BCnetwork (b). In the third processing route, the BC growing medium is modified by the addition of aGO suspension and the BC network is synthetized in the presence of GO (c). For the fourth processingroute a conventional growing medium is used to grow a first BC pellicle. Then, a modified growingmedium is prepared adding a GO suspension. This modified medium is sprayed onto the first BCpellicle forming a thin layer of culture medium on which new BC nanofibres are synthetized in presenceof GO (d).

For instance, Fang et al. [35] prepared BC-GO membranes following the first route (Figure 1a) forselective ion permeation. They dried and disintegrated the pristine BC pellicle. Then, they dispersed itin formamide with sonication for 2 h at 400 W to prepare stable BC dispersion with concentration of1 mg mL−1. 15 mL of the BC dispersion was mixed with 5 mL of a GO dispersion and sonicated for10 min. Then the mixture was vacuum filtrated to prepare BC and BC/GO membranes.

The disintegrated BC network can easily undergo chemical treatment. Liu et al. [41] prepared aBC-GO cross-linked nanocomposite by a one-step esterification process. They prepared a dispersion offreshly exfoliated GO sheets and disintegrated BC pellicles in anhydrous N,N-dimethyl formamide(DMF). Dicy clohexyl carbodiimide (DCC) was added as a dehydration reagent. The esterificationbetween carboxyl groups of GO and hydroxyl groups of BC was conducted under nitrogen atmosphereat 70 ◦C 1 for 48 h to create the cross-linking BC/GO networks. Then, the reaction mixture was filteredthrough a nylon membrane, rinsed with ethanol and deionized water. The film was finally air-dried atroom temperature.

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The third route shown in Figure 1c is performed by modifying the culture medium of BC byadding a BC suspension in it. The bacteria synthetize the BC fibres in the presence of the GO plateletsand a BC pellicle obtained has GO platelets incorporated in the BC network without any furthertreatment [42–45]. Compared with the first route (Figure 1a), when using undisturbed BC membranesthere is no need of energy-intensive disintegration process or BC solubilisation in organic solvents/ionicliquids [46], which could have issues related to environmental toxicity and biocompatibility. In addition,the disintegration of BC reduces the mechanical strength and damages the integrity of the BC network.However, incorporating GO platelets into the 3D BC network could be a challenging task, especiallywhen the sample thickness is large (ca. 3 mm) [47].

In order to overcome the difficulties of incorporating graphene into the BC network, a novellayer-by-layer self-assembly route (Figure 1d) has been proposed [47–50]. First, a conventional growingmedium is used to grow a first BC pellicle. A modified growing medium is prepared adding a graphenesuspension. Then, this modified medium is sprayed onto the first BC pellicle forming a thin layerof culture medium on which new BC nanofibres are synthetized in presence of graphene platelets.This process is repeated several times until the desired thickness is achieved. This layer-by-layer methodresults in the formation of mechanically strong and thick three dimensional BC-GO network [50].

Some modifications have been proposed to the aforementioned routes when a third phase isincorporated to form novel BC-GO hybrid nanomaterials. For instance, Chen et al. [51] used anin-situ synthesis of PEDOT (poly-3,4-ethylenedioxythiophene) to prepared BC-GO-PEDOT conductivefilms. They immersed a dry BC pellicle into an 3,4-Ethylenedioxythiophene (EDOT)- FeCl3 ethanolsolution). During the ethanol evaporation, the EDOT monomer started to form a PEDOT shellon the surface of the BC nanofibres. Then, a GO solution was dropped onto the BC-PEDOT filmby spin−spray method. Wan et al. [52] and Luo et al. [48] have also made a hybrid nanomaterialusing a conductive polymer. They first prepared a BC-GO nanocomposite using the layer-by-layerself-assembly route. Then, they immersed this BC-GO nanocomposite in a HCl aqueous solutioncontaining aniline monomer. The solution was vigorously agitated for 24 h. An ammonium persulfatesolution was added drop- wise to promote the in-situ oxidative polymerization of aniline on the surfaceof the BC-GO nanocomposite to obtain a BC-GO-PANI hybrid. Other conductive polymers, such aspolypyrrole and polyethylenimine have also been in-situ polymerized on BC-GO nanocompositesfollowing similar processing routes [53,54].

The BC-GO nanocomposites can be produced as hydrogels, films or aerogels. BC is synthetized bybacteria as a network of nanocellulose fibres that hold a large amount of water. BC-graphene hydrogelscan be obtained modifying the bacteria culture medium without further processing. When a membraneor film is needed, water is extracted from the BC network by air-drying, hot- and cold-pressing orvacuum-filtration. BC-GO aerogel can be prepared from BC-based hydrogels by freeze-drying or by asupercritical CO2 method [55–57].

3. Applications of Bacterial Cellulose-Graphene Nanocomposites

3.1. Electronic and Energy Storage Devices

Single graphene layers have the highest known electrical conductivity [58]. Many researchershave used graphene as filler to prepare conductive polymer matrix composites [59–61], in spite ofthe fact that polymers are electric insulators. It has been reported that the incorporation of graphenecan lead to a percolation behaviour at very low volume fractions and can increase the conductivity ofthe resulting composites by several orders of magnitude [62–64]. It has been reported that polymericcomposites reinforced with carbon nanofillers, such as carbon nanotubes and graphene, feature anelectric tunnelling effect. If the polymer layer between carbon intrusions is thing enough (~1–2 nm)electrons can cross and current can flow between both inclusions [65–67].

RGO has been incorporated to a BC matrix in order to prepare conductive paper and films [52,68–71].Ccorahua et al. [70] reported the incorporation of graphene into a pristine BC network by vacuum

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filtration. The dependence of the electric conductivity on the amount of graphene incorporatedsuggested the existence of a critical content of RGO that boosted the conductivity of the BC-RGOnanocomposite. The conductivity of BC-RGO was dependent on the GO content. At an RGO content of20% the conductivity was 1 S·m−1. At an RGO content of 30%, the conductivity was 12 S·m−1. Table 2shows the electric conductivity of several BC-graphene composites reported in the literature.

Table 2. Conductivity of BC-graphene nanocomposites reported by different studies.

Nanocomposite Graphene Content (%) Conductivity (S·m−1) References

BC-Graphene 18.4–26.8 70–80 [49]BC-RGO 2.5–10 0.001–0.01 [69]BC-RGO 30 12 [70]

BC-Graphene-PANI - 170 [52]BC-RGO-NH4I 30 0.013 [71]

These conducting BC-graphene based materials can potentially be used in the assembly of novelenergy storage devices. Supercapacitors are among the most promising energy storage devices andare capable of managing high power rates compared to batteries. However, they are not able to storethe same amount of charge as batteries [72]. Supercapacitors are, thus, suitable for applications inwhich power burst are needed but storage capacity is not required. The advantages of supercapacitorsinclude their ability to charge and discharge in an extremely short period of time (seconds) andtheir long cycle life. There are different types of supercapacitors. Among them, the electrochemicaldouble-layer capacitors (EDLCs) are the most promising type of capacitor to be developed usingBC-graphene nanocomposites.

In a traditional electrostatic capacitor (Figure 2a), energy is stored via an electrostatic fieldgenerated from the removal of charge carriers (i.e., electrons) from one metal plate (i.e., electrode),then depositing them on another [73]. Their charge mechanism does not involve irreversible chemicalreactions (there is no Faradic process). Rather, the charges are physically attached on the surface of theelectrodes in an electric double layer [74]. EDLCs work much in the same way as electrostatic capacitors(Figure 2b) but using electrodes with a very high surface area. As the capacitance is proportional to theelectrode area, EDLCs achieve very high capacitance values (kilo-Farads) compared to electrostaticcapacitors (mili- and micro-Farads) [74].Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 7 of 19

Figure 2. Schematic representation of an electronic capacitor (a) and a flexible electrochemical

double-layer capacitor (EDLC) (b).

The electrodes of conventional EDLCs are formed by a layer of activated carbon paste deposited onto a metallic current collector. A metallic casting encases the electrodes immersed in a liquid electrolyte (Figure 2a). However, the large micro/macropores within activated carbon is disadvantageous for the adsorption of the electrolyte on the surface of electrodes, deteriorating the function of EDLCs. In addition, for some emerging applications such as wearable electronics, electronic newspapers and paper-like mobile phones [75], conventional EDLCs are heavy and are incompatible with large strains.

Freestanding conductive films are considered to be one potential solution to address the challenge of producing flexible capacitors. Carbon-based paper-like materials, such as RGO paper and carbon nanotube (CNT) paper are potential candidates to be used as flexible electrodes because of high their conductivity and large specific surface area [61]. However, the small mass loading that can be achieved limits their potentials. An alternative solution has been found incorporating graphene on a flexible, porous and light-weight BC substrate. The BC substrate can provide three-dimensional (3D) porous network structure and therefore enable high mass loading. The excellent mechanical properties of BC [76] provide the BC-based electrodes with high mechanical integrity upon bending or folding. Figure 2b shows a schematic representation of an all-Solid-State flexible supercapacitor in which BC-graphene nanocomposite films are used as electrodes.

Several works report the use of BC-graphene nanocomposite films for the production of flexible and highly-efficient supercapacitor electrodes. Table 3 shows that these nanocomposites films exhibited high electrical conductivity (171–1660 S m−1) and large specific capacitance (160–556 F g−1), compared to activated carbon-based electrodes, along with high cycling stability (86%–100% retention).

Table 3. Conductivity, specific capacitance and cycling stability of flexible electrodes prepared from BC-graphene nanocomposite films.

BC-Graphene System Conductivity (S m−1)

Specific Capacitance

(F g−1)

Cycling Stability

(%) Reference

BC/GO 171 160 90.3, after

2000 cycles [41]

BC/GE/PANI 1660 645 82.2%, after 1000 cycles

[48]

Polypyrrole/Bacterial Cellulose/Graphene 1320 556 95.2, after

5000 cycles [36]

BC/RGO - 216 86, after

10,000 cycles [34]

Figure 2. Schematic representation of an electronic capacitor (a) and a flexible electrochemical double-layercapacitor (EDLC) (b).

The electrodes of conventional EDLCs are formed by a layer of activated carbon paste depositedonto a metallic current collector. A metallic casting encases the electrodes immersed in a liquid electrolyte

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(Figure 2a). However, the large micro/macropores within activated carbon is disadvantageous forthe adsorption of the electrolyte on the surface of electrodes, deteriorating the function of EDLCs.In addition, for some emerging applications such as wearable electronics, electronic newspapers andpaper-like mobile phones [75], conventional EDLCs are heavy and are incompatible with large strains.

Freestanding conductive films are considered to be one potential solution to address the challengeof producing flexible capacitors. Carbon-based paper-like materials, such as RGO paper and carbonnanotube (CNT) paper are potential candidates to be used as flexible electrodes because of high theirconductivity and large specific surface area [61]. However, the small mass loading that can be achievedlimits their potentials. An alternative solution has been found incorporating graphene on a flexible,porous and light-weight BC substrate. The BC substrate can provide three-dimensional (3D) porousnetwork structure and therefore enable high mass loading. The excellent mechanical properties ofBC [76] provide the BC-based electrodes with high mechanical integrity upon bending or folding.Figure 2b shows a schematic representation of an all-Solid-State flexible supercapacitor in whichBC-graphene nanocomposite films are used as electrodes.

Several works report the use of BC-graphene nanocomposite films for the production of flexibleand highly-efficient supercapacitor electrodes. Table 3 shows that these nanocomposites films exhibitedhigh electrical conductivity (171–1660 S m−1) and large specific capacitance (160–556 F g−1), comparedto activated carbon-based electrodes, along with high cycling stability (86%–100% retention).

Table 3. Conductivity, specific capacitance and cycling stability of flexible electrodes prepared fromBC-graphene nanocomposite films.

BC-Graphene System Conductivity(S m−1)

Specific Capacitance(F g−1)

Cycling Stability(%) Reference

BC/GO 171 160 90.3, after 2000 cycles [41]

BC/GE/PANI 1660 645 82.2%, after 1000 cycles [48]

Polypyrrole/BacterialCellulose/Graphene 1320 556 95.2, after 5000 cycles [36]

BC/RGO - 216 86, after 10,000 cycles [34]

Nitrogen-Doped CarbonNetworks/Graphene/Bacterial Cellulose - 263–318 ~100, after 20,000 cycles [77]

Batteries are other energy storage devices that can also been constructed using bacterialcellulose-graphene based nanocomposites. For instance, Shen et al. [40] used pyrolized BC toprepare a nanocomposite with GO for the development of a new Li–S battery. They used the pyrolizeBC/GO nanocomposite as a membrane separator placed between the anode and the cathode of thebattery. The 3D structure of this BC/GO nanocomposite worked as an effective barrier to retardpolysulfide diffusion during the charge/discharge process to enhance the cyclic stability of the Li–Sbattery. Such Li-S batteries exhibited a specific capacity of nearly 600 mAh.g−1 and only 0.055% capacitydecay per cycle over 200 cycles. Zhang et al. [78] also used BC-GO membranes as separators for redoxflow batteries. They found that the batteries assembled with BC-GO separators had a charge-dischargeprofile similar to that of the batteries equipped with commercial Nafion 212 membranes and achieve astable cycling performance with a Coulombic efficiency of ∼98%.

BC-graphene based nanocomposites have also been used to produce other electronic devices suchas sensors and actuators. The amperometric response of BC-GO based nanocomposite films has beenused to fabricate sensors. Zhang et al. [79] prepared a modified glassy carbon electrode by drop-castinga BC-GO suspension onto the surface of glassy carbon. This modified glassy carbon electrode was usedto determine nitrite concentration in water, in a wide linear range of 0.5 to 4590 µM with detection limitand sensitivity of 0.2 µM and 527.35 µA µM−1

× cm−2, respectively. Lv et al. [80] used the layer-by-layerprocessing route (Figure 1d) to incorporate nitrogen doped graphene oxide quantum dots (N-GOQDs)in a BC network. This BC/N-GOQD nanocomposite were used for the detection of iron ions in aqueoussolutions. Their results showed that the blue-emitting BC/N-GOQD fluorescent probes exhibited a

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sensitive response to Fe3+ within a concentration range of 0.5–650 µM with a lower limit detectionof 69 nM. Hosseini et al. [81] prepared a BC/RGO conductive aerogel by a supercritical CO2 (ScCO2)drying method. They characterized the mechanical and electrical properties of the BC/RGO aerogelsand found a gauge factor (ratio between the relative change in electrical resistance to the mechanicalstrain). This suggests that such a BC/RGO aerogel can effectively be used as a strain sensor.

Kim et al. [82] prepared a bioelectronic soft actuator using 2,2,6,6-tetramethylpiperidine-1-oxylradical-oxidized bacterial cellulose (TEMPO-BC) and graphene. The top and bottom surfaceof the TEMPO-BC/graphene film was coated with a conducting electrode made from poly(3,4-ethylenedioxythiophene) polystyrene sulfonate (PEDOT:PSS). The results showed that under sinusoidalexcitation of 1.0 V at 0.1 Hz, the tip displacement of the TEMPO-BC/graphene actuator reached peaktip displacements of ±2.5 and ±4 mm, while the displacement of the TEMPO-BC actuators reached apeak of ±1.2 mm. The unique TEMPO-BC/graphene actuator showed large static deformation withoutapparent back-relaxation, much faster response time and highly durable harmonic actuation comparedwith other biopolymer actuators.

3.2. Sorbent Nanocomposites for Water Purification

BC-graphene nanocomposites have also been used in the construction of devices for the purificationof water, specifically for two types of applications—water-oil separation and metal ions removal.BC-graphene aerogels have been developed as efficient low-cost absorbents that can potentially beused in the removal of crude oil, petroleum products and toxic organic solvents. Traditional absorbentsinclude foams and powders with high absorption capacity, fast absorption kinetics, selectivity andcontrollable hydrophobicity [83]. The absorption capacity of these materials is dependent on a varietyof physicochemical properties such as density, surface tension, viscosity, polarity, hydrophobicity,porosity and pore size [47].

Carbonaceous materials such as activated carbon, expanded perlite, zeolites and three-dimensional(3D) porous carbon nanotube-based materials have been applied as absorbents due to their low apparentdensity, high porosity, large specific surface area, intrinsic surface hydrophobicity and superwettabilityfor organic solvents and oils and environmental friendliness [84]. For instance, Gui et al. [85] developeda carbon nanotube sponge that could absorb various solvents and oils with an absorption capacity upto 180 times of their own weight.

As shown in previous sections there are a variety of processing techniques used to prepare BC-GOnanocomposite aerogels. However, due to strong interaction of GO with water, these BC-GO aerogelscannot be used for the specific separation of oily compounds. Wang et al. [86] reported a method inwhich BC-GO aerogels underwent further reduction in H2 flow leading to BC-RGO nanocompositeaerogels, which exhibited specific absorption only for organic liquids. These nanocomposite aerogelscould specifically absorb 135–150 g organic liquids per g of their own weight.

Luo [56] followed a different approach. They first freeze-dried a BC-graphene pellicles inorder to obtain aerogels. Then, the aerogels were carbonized at 800 ◦C for 2 h in a tubular furnace.The carbonized BC-graphene nanocomposite aerogel featured a honeycomb-like surface morphologyand a three-dimensional (3D) interconnected porous structure. They showed high absorption capacitiesfor a wide range of oils and organic solvents, including hexane, acetone, methanol, diesel oil, siliconeoil, pump oil and soybean oil, among others. The maximum value absorption value reached was of457 g of silicone oil per g of their own weight. This high absorption capacity is due the fact that thehoneycomb-like surface provides sufficient space and active sites improving the efficiency of liquiddiffusion and the hydrophobic interactions between absorbates and carbon.

On the other hand, BC-graphene membranes have been used as adsorbents for metal ionsremoval [35,87]. According to the Environmental Protection Agency (EPA), metal ions such aslead (Pb2+), zinc (Zn2+), cadmium (Cd2+), manganese (Mn 2+), silver (Ag+) and mercury (Hg2+)are important water pollutants from industries such as metallurgy, pharmaceutical, chemical and

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petroleum refining industry [88]. This represents an important threat to humans and aquatic and otherlife forms.

A variety of technologies have been developed to perform metal ion removal, including reverseosmosis, ultrafiltration, ion exchange, coagulation, floatation, chemical precipitation, electrodialysis,flocculation and evaporative recovery [89]. Among them, adsorption has the advantage of beingessentially toxic-free, low cost, flexible and simple to operate [90]. Adsorption is a phenomenon inwhich pollutant metal ions associate with ions that are peripherally available on the adsorbent material.

Both, BC and graphene have been used in the development of adsorbent devices for waterpurification. BC has been shown to be able to receive guest molecules or inorganic particles [91–93].BC nanocomposites and hybrid materials have been reported as adsorbent materials, especially forheavy metals [94–97]. Graphene oxide (GO) has oxygen-containing functional groups (i.e., hydroxyl,carbonyl, carboxyl and epoxide) on the surface, enabling them to form strong complexes with metalions. Thus, GO can be used as an adsorbent for heavy metal ions and dyes [98]. It has been reportedthat electrostatic interaction is the mechanism behind the cationic heavy metal remediation; betweenmetal cations and negative surface charge and/or electrons of GO-based materials [99].

Mensah et al. [87] prepared an adsorbent membrane by esterification of bacterial cellulose (BC)and graphene oxide (GO), containing hydroxyl, alkyl and carboxylate groups. The results showed thatthe BC-GO samples prepared have a specific surface area of 49.99 m2/g and an average pore size of18.696 Å with a total pore volume of 0.0356 cm3/g. Batch experiments–adsorption studies confirmed thematerial to have a very high Pb2+ removal efficiency of over 90% at pH 6–8. The maximum adsorptionwas 214.3 mg/g for the 60 mg/L initial concentration of Pb(II) ions. Fang et al. [35] also prepared BC-GOmembranes for ion adsorption. The BC-GO membrane prepared was shown to have selective ionpermeation according to the size of ions. They found that ions of K+ and Cl− with small size (hydratedradii < 4 Å) can quickly diffuse through the BC-GO membrane while RhB with large ion size (hydratedradius > 1 nm) cannot. This suggests that this BC-GO nanocomposite membrane could be used notonly for water purification but also as a selective ion permeation device.

3.3. Bacterial Cellulose-Graphene Nanocomposites for Biomedical Applications

BC has been shown to be a biocompatible and non-toxic material with potential applications inthe biomedical field [3,4,100]. Novel BC-based nanocomposites have been developed for a varietyof biomedical applications including scaffolds for tissue engineering [101–103], skeletal and softtissue grafts [104,105], wound dressing patches [106], drug delivery devices [107] and artificial bloodvessels [108], among others.

Graphene has also been used for biomedical applications such as antibacterial materials [109,110],drug delivery systems [111,112] and tissue engineering scaffolds [113,114]. However, it has beenreported that graphene-based nanomaterials may have toxic effects on cells and tissues. In general,nanoparticles can enter cells, if they are <100 nm in diameter. They can enter the nucleus, if they are<40 nm in diameter [115]. GO sheets can interact with cells, adhere the cell membrane and insert in thelipid bilayer. This interaction can impair cell membrane integrity and alter its functions such as theregulation of membrane associated genes, fluidity and ion channels [116].

Several factors can determine the biocompatibility of graphene-based materials, including size,surface area, surface modifications, charge and the formation of agglomerations [117–119]. Some studiessuggest that graphene-based materials are biocompatible for a specific biomedical application [120–122].Some researchers have improved the biocompatibility of graphene-based materials and prevent theinflammatory response using purified graphene oxide dispersions [123] or functionalizing GO withpoly(acrylic acid), which can modify the composition of the protein corona formed on the GO surfacewhich determines its cell membrane interaction [116]. When novel graphene-based materials aredeveloped for biomedical applications, biocompatibility must be considered, including accurate studiesof their potential toxicity effects.

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Table 4 shows the biocompatibility tests performed for BC-graphene nanocomposites prepared to beused in a variety of biomedical applications. The results are not comparable because they were performedusing different methodologies and cell lines. However, the authors reported fairly good biocompatibilityresults. The biomedical applications reported for BC-graphene nanocomposites include cell culture [45],tissue engineering [68,124,125], wound dressing [126] and drug delivery [111,127–129].

Table 4. Biocompatibility of BC-graphene based nanocomposites tested for different biomedical applications.

Type of Matrix Type of Graphene Biocompatibility Test Viability (Cells) Potential ApplicationAssessed Reference

BC hydrogel Graphene oxide(GO)

Mouse fibroblast cell line(L929), CCK-8 assay

0.55–1.1 (O.D. = 450nm †) Drug delivery system [129]

BC hydrogel pellets Graphene oxide(GO)

Mouse peritonealmacrophages-RAW264.7,

MTT assay~75 × 104 cells (72 h) Drug delivery system [44]

BC film Reduced grapheneoxide (RGO)

Human marrowmesenchymal stem cells

(hMSCs)~5.5 × 104 cells (72 h) - [45]

BC/Hydroxyapatiteporous structure

Graphene oxide(GO)

MG-63 and NIH 3T3 cells,MTT

110–120%(MG-63 cells, 24 h)

80–110%(NIH 3T3 cells, 24 h)

Tissue engineering [124]

BC/PEDOT film Graphene oxide(GO) PC12 neural cells, MTT 95% (24 h) Regenerative medicine [51]

BC hydrogel Graphene oxide(GO) Human dermal fibroblast 80% (24 h) Wound dressing [126]

† O.D.: Optical density, absorbance.

4. Conclusions

Bacterial cellulose is a biopolymer synthetized by bacteria as a coherent 3D network of cellulosenanofibres. This network has remarkable mechanical properties and has been used as matrix forthe preparation of nanocomposites for a variety of different applications. Graphene nanomaterials,including pristine single graphene sheets, graphene oxide and reduced graphene oxide have been usedto provide polymeric materials with novel properties such as electric conductivity, absorption andadsorption capabilities. In order to take advantage of the intrinsic properties of both, bacterial celluloseand graphene, many processing techniques have been developed to successfully incorporate graphenenanomaterials, mainly graphene oxide and reduced graphene oxide. Films, membranes, hydrogels andaerogels can be produced using a variety of processing routes. The three main applications identifiedfor these nanocomposites were the development of novel electric conductive materials and energystorage devices, the preparation of aerogels and membranes for the removal of oil and metal ions fromwater and a variety of biomedical applications. The incorporation of graphene has shown to greatlyimprove the conductivity of BC-based materials, making BC-graphene nanocomposites suitable for theassemblage of novel flexible supercapacitors that could be used for energy storage of novel flexibleelectronic devices. Regarding the biomedical applications, BC-graphene nanocomposites have beenused in the preparation of materials for cell culture, tissue engineering, wound dressing and drugdelivery. However, there are reports showing that graphene can be toxic for cells and tissues. Furtherinvestigations should be focused on the biocompatibility of these novel BC-graphene nanocompositesfor biomedical applications.

Author Contributions: Conceptualization, O.P.T. and F.G.T.; investigation, O.P.T. and F.G.T.; writing—originaldraft preparation, O.P.T.; supervision, F.G.T. All authors have read and agreed to the published version ofthe manuscript.

Funding: This research was funded by FONDECYT-CONCYTEC, grant number 063-2018-FONDECYT-BM.

Conflicts of Interest: The authors declare no conflict of interest.

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Abbreviations

BC Bacterial celluloseCNT Carbon nanotubesDCC Dicy clohexyl carbodiimideDMF N,N-dimethyl formamideEDLC Electrochemical double-layer capacitorGFN Graphene family nanomaterialsGO Graphene oxideN-GOQD Nitrogen doped graphene oxide quantum dotsPANI PolyanilinePEDOT Poly-3,4-ethylenedioxythiopheneRGO Reduced graphene oxideTEMPO-BC 2,2,6,6-tetramethylpiperidine-1-oxyl radical-oxidized bacterial cellulose

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